Evolution & Morphology in the Homobasidiomycetes
by Gary Lincoff & Michael Wood
Nearly every amateur mycologist and many professional mycologists, especially those not engaged in systematics, see mushrooms much the way they have been understood, described and classified for over 200 years. The standard modern approach to the basidiomycetes has been that of Elias Fries' 1874 Hymenomycetes Europaei. There, excluding the rust and smut fungi and the traditional gasteromycetes, Fries divided all the basidiomycetes into 6 major groups based on the shape of the fruiting body (sporocarp) in the field. These shapes include mushrooms containing (1) gills, (2) pores, (3) teeth, (4) vase, parchment or crustlike fruiting bodies, (5) coral-like fungi, and (6) tremelloid or jelly-like mushrooms.
Each of these shapes is very much like what in zoology has been referred to as a "bauplan." That is, there are a discrete and limited number of body shapes that unrelated groups of organisms have evolved, depending on environmental conditions. Another name for this is "convergent evolution." This is conspicuous in plants where, for example, we see cacti in the American southwest and their vegetatively similar counterpart, the Euphorbias in Old World desert habitats. In mammals, the marsupials, as an Order, have diverged to fill nearly all the niches in Australia that at least five different Orders of mammals fill in the rest of the world: the kangaroo, koala, wombat, Tasmanian Devil, banded anteater, marsupial "shrew", and so on, resemble mammals in the New World among the rodents, insectivores, anteaters, carnivores, and primates. In fungi, the gill, as a structure on which to develop spores, has evolved many times by unrelated groups of mushrooms. The same is true of the pore, the spine (or tooth), the coral-like structure, the vase, parchment or crustlike structures, and the tremelloid or jellylike fruiting body. In addition, the gasteromycetes, which used to be thought to be a coherent group based on a fruiting body that remained enclosed until it was mature, has been shown to contain taxa more closely related to many of the mushrooms with gills, pores, teeth, and so on, than to one another. Seen as such, the gasteromycetes, however useful the group concept is in the field, has ceased to exist as an evolutionary unit because the mushrooms that compose it all evolved from different and unrelated ancestors.
Mushroom Identification & Classification
At the risk of oversimplifying the development of taxonomy in mycology over the past two hundred plus years, there are two main traditions in which mushrooms have been identified and classified.
The 19th Century Friesian field-based approach to identifying and classifying mushrooms, is the one we still primarily use in our field guides, on our mushroom foray display tables, at our mushroom fairs, and on our club checklists, if they're not just alphabetical by genus and species. This tradition actually predates Fries, since Persoon's 1801 Synopsis Methodica Fungorum offered an approach that Fries both simplified and amplified over a very long career. Subsequent modifications of a classification determined solely by the mushroom shape, but based here and there on microscopic characters or chemical reagent reactions, have produced a somewhat less artificial arrangement of the fungi, but also one more confusing to beginners.
The other tradition, the Patouillardian dates back before 1900, but that year saw the publication of Patouillard's Essai taxonomique, the first guide to use microscopic characters systematically. The result was a major rearrangement of the basidiomycete fungi, achieved by de-emphasizing the field-based characters and giving the microscopic characters a central role in determining classification. So effective has this approach been that 5 of the 8 major clades of homobasidiomycetes, as determined by DNA sequencing (and displayed here on the accompanying chart), were already partially understood by Patouillard and his pre-DNA taxonomy. The 20th Century saw this systematic microscopic approach, developed by the French, eventually picked up and extended by mycologists in the U.K., Germany, and the U.S. One of the most prominent of the mycologists from this era has been Rolf Singer, whose Agaricales in Modern Taxonomy has served as the model for modern pre-DNA taxonomic research.
In just the last 20 years or so a new technology (DNA sequencing techniques with PCR [polymerase chain reaction]) and a new methodology (Cladistics) for arranging and presenting data have been worked out, first for animals and plants, and now for mushrooms. Phylogenetic trees (cladograms) attempting to show in a visual way the evolutionary relatedness among diverse fungi have been developed for many groups of mushrooms. Different regions of sequenced DNA or different methodologies for presenting this data, however, have led to different phylogenies (cladograms). David Hibbett, in constructing phylogenies of the homobasidiomycetes (see accompanying chart), uses nuc-lsu rDNA (nuclear large subunit ribosomal DNA) sequences. Tom Bruns uses the ITS (internal transcribed spacer region) molecule in his research. Still others use nuclear and mitochondrial small subunit and large subunit ribosomal DNA sequences. Some sequences, e.g., ITS, appear to be good at the species level for some groups of fungi; others, e.g., nuc LSU, at higher taxa levels. Still others are used to discern trends in morphological evolution rather than for identifying or classifying mushrooms.
These two traditions, field-based and DNA-based, serve different communities. The field-based approach is designed for use by non-researchers and is intended for the identification (or recognition) of the mushrooms we find in the field. A premium is placed on stability so that what has been learned can be found conveniently in a classification that remains essentially the same over time. The DNA-based approach is designed for use by researchers and intended for facilitating the testing of hypotheses about the relationships between and among groups of fungi. A premium is placed on flexibility so that any classification used has to be able to accommodate change when needed, however large and however often.
If one of the primary purposes of classification is the storage and retrieval of information, information that can be stored and retrieved by anyone without a specialized education, then this field-based arrangement of organisms is a very practical, attractive, and convenient solution to the problem of achieving some degree of order in the apparent chaos of creation. If the primary purpose of classification is to reflect genealogy (phylogeny) or evolutionary relatedness, then the information stored and retrieved is only readily available to those with a specialized education and special lab equipment.
Using just field characters or just DNA sequences to identify and classify mushrooms, as this chart represents them, are both, in a sense, artificial solutions to the problems confronting the taxonomist.
Using just field-based characters, for example, puts all mushrooms with gills together in a single group, however many subgroups we choose to recognize. It also separates all these gilled mushrooms from all other fungi lacking gills. The same holds true for putting together all mushrooms with pores, or with teeth, or putting together all coral-like fungi or all parchment and crust fungi. We now see, by using a variety of modern techniques, that all these morphotypes have evolved many times from different evolutionary lineages. That is, a gilled mushroom might be more closely related to a bolete, a tooth fungus or a coral mushroom than to another gilled mushroom. And so on.
Using just DNA sequencing data puts together in the same clade mushrooms that appear in the field to be totally unrelated and excludes others that appear from field characters to be closely related. For example, in the Euagarics clade, some gilled mushrooms, but not others, are placed together with the coral genus Clavaria, the parchment genus Chondrostereum, and some, but not all, puffballs, etc.
Unlike the field-based approach that invites us to make the very common mistake that appearance is reality when it is just another example of convergent evolution, the DNA approach leaves us to assume homologous evolution, that is, evolutionary relatedness, when there is no other supporting data except for the DNA sequences. Placing Stereum with Russula or Rickenella with Hymenochaete is asking us to accept something for which there are no apparent correlative characters to support the hypothesis, which nevertheless may be correct.
In a sense, both the field-based and the DNA approaches rely on single-character taxonomy, the silver bullet approach, for mushroom identification and classification. Field-based taxonomy is based on the belief that we can identify mushrooms, much as can identify plants and animals, with no special education or equipment. This was the basis of McIlvaine's 1900 "1000 American Fungi." DNA-based taxonomy is based on the belief that we can identify any organism by finding its bar code. A DNA bar code, as the Bar Code of Life website has it, is "a short DNA sequence enabling discrimination of species within a given compartment of life." There is an article in New Scientist (June 26, 2004) about this. There is even a consortium of bar coders developing protocols for different disciplines.
It's very appealing to believe that a simple test will tell us what we want to know, but taxonomists of the "old school" and systematists of the "new school" both know that life's diversity is more complex than this suggests. In fact, the traditional criterion for the best classification might still be the best: it should be based on the greatest number of possible characters; that is, field-based characters, microscopic characters, macro- and microscopic chemical characters, and, now, DNA sequences. This used to be called "correlation of characters" taxonomy. Whatever path you follow, however, caveat emptor still applies.
The Clades: What's In and What's Not
This clade includes nearly all the gilled mushrooms. In addition, it includes the coral (Clavaria), the tooth fungus (Deflexula), the polypore (Fistulina), the cantharelloid fungus (Cantharellula), the parchment (Chondrostereum), and the gasteroid fungi: the gasteroid agarics like Endoptychum, the true puffballs (Calvatia & Lycoperdon), the stalked puffballs (Battarrea & Tulostoma), and the bird's nest fungi (Crucibulum & Cyathus). It also includes many cuplike (or cyphelloid) 'agarics,' like Cyphella and Calyptella. It even includes Nia vibrissa, a puffball-like marine basidiomycete!
Gilled mushrooms not in this clade include: Lactarius & Russula, Lentinellus (Russuloid clade); Gomphidius & Chroogomphus, Paxillus & Tapinella, Hygrophoropsis (Bolete clade); Horakia (Thelephoroid clade); Rickenella & Loreleia (Gerronema) marchantiae (Hymenochaetoid clade); Lentinus & Panus (Polyporoid clade); Cantharellus (Cantharelloid clade); and Gloeocantharellus & Gomphus (Gomphoid-Phalloid clade).There are gilled or agaricoid mushrooms in every major phylogenetic clade!
This clade includes all the mushrooms we call boletes. In addition, it also includes the gilled mushrooms Gomphidius & Chroogomphus, Paxillus & Tapinella, Phylloporus, and Hygrophoropsis. It includes the coral mushroom Clavulinopsis, the crust fungi Serpula and Coniophora, a toothed crust Hydnomerulius pinastri, and a variety of "gasteromycetes," e.g., Scleroderma, Astraeus, Pisolithus, Calostoma, Rhizopogon, and Truncocolumella. It even includes the pagoda fungus Podoserpula pusio.
In addition to Lactarius and Russula, this clade includes all the gasteroid forms of these mushrooms, like Macowanites and Zelleromyces. In addition, it includes the gilled mushroom Lentinellus, the tooth fungi Auriscalpium and Hericium, the coral mushroom Clavicorona, the polypores Albatrellus and Bondarzewia, and the crust or parchment fungi Aleurodiscus and Stereum.
This clade includes the vase fungus Thelephora, the tooth fungi Hydnellum and Sarcodon, the cantharelloid fungus Polyozellus, the coral Scytinopogon, the polypore Boletopsis, the crust fungi Tomentella and its allies, and the lamelloid fungus Lenzitopsis.
This clade contains most of the polypores, plus the gilled mushrooms Lentinus and Panus, the chanterelle-like Faerberia carbonaria, the coralloid fungus Sparassis, the tooth-like fungi Irpex lacteus and Phanerochaete chrysorhiza, the crust fungus Phlebia, even the hydnoid-thelephoroid fungus Mycobonia, and the little, white craterellus-like Stereopsis humphreyi.
This is a small clade that includes a few polypores, like Coltricia, Inonotus, Oxyporus and Phellinus, as well as Trichaptum, and the toothed Hydnochaete, the vaselike Cotylidia, the crust Hymenochaete, and the gilled mushrooms Rickenella and Loreleia (Gerronema) marchantiae.
This clade includes the genera Cantharellus and Craterellus, plus the coral fungi Clavulina and Multiclavula, the tooth genus Hydnum, and the resupinates Sistotrema and Botyrobasidium. It may even include the heterobasidiomycete jelly crust, Tulasnella!
This clade includes Gomphus and Ramaria, and Clavariadelphus, plus all the stinkhorns, as well as the earthstar, Geastrum, the cannonball bird's nest, Sphaerobolus, the tooth Beenakia, the crust Kavinia and the gasteroid Gautieria and Hysterangium.
It is also worth noteing that many of the Heterobasidiomycetes (Jelly Fungi) also have the same general morphologies as the Homobasidiomycetes discussed here. The Jelly Fungi do not form a single clade but includes all the fungi that are traditionally recognized in the 3 main orders of the Auriculariales, Dacrymycetales, and Tremellales. It includes examples of all the basic mushroom shapes: jelly (Tremella), coral (Calocera), tooth (Pseudohydnum), pore (Aporpium), cantharelloid (Phlogiotis), parchment (Auricularia mesenterica) gasteromycete-like (Phleogena), cuplike (Auricularia auricula), and even gill-like (Protodaedalea).
About the Chart
This chart is being presented so that those with no specialized knowledge of the fungi can make sense of the mushrooms they find by reading the chart horizontally. In this way, they can see collected together the mushrooms they know and, at the same time, by looking vertically, they can see what groups (clades) the mushrooms belong in as seen by DNA sequencing data. For those with specialized knowledge, the vertical assemblage of the major clades is understandable, but the horizontal assemblage of the body shapes (or dominant bauplans) may elude the specialist who only studies the DNA data.
A glance at the chart will show, as no list can, that nearly every body plan (gill, pore, tooth, etc.) has been used by every major clade or evolutionary lineage of basidiomycetes. [Although the traditional Jelly Fungi are conspicuous by their absence here, they also reflect this trend, and many common field guides display this by showing jelly fungi that are coral-like, tooth-like, vase-like, crust-like, and so on. As these lineages are resolved to our satisfaction they will be added to this chart.] Empty boxes in the chart may simply mean that examples have yet to be found or confirmed. Like Mendeleev's Periodic Table of the Elements, we can expect that the many or most of the blanks on this chart will fill in with time.
On the accompanying chart, if you look at the mushroom names following the shapes "gills," "pores," "teeth," "coralloid," and "parchment / crust," for example, you will see many names that you know and some that you've never heard of before. While we have used as many familiar names of the genera as we could, there are genera of mushrooms known only from the tropics or from outside the Americas. Or, they may be local mushrooms that have had their names changed recently. Just two centuries ago these five "groups" of mushroom shapes (or morphotypes) would have had all their species placed in just five genera: Agaricus, Boletus, Hydnum, Clavaria, and Thelephora. Today, there are more than 500 genera containing the species found in these 5 morphotypes. The reasons for all these name changes are many, but the benefits are believed to far outweigh the difficulties and frustration caused by all the name changing. When you encounter a name that you don't know or can't find in one of your mushroom guides, one solution is to go to IndexFungorum and type in the name of the genus. There, with a couple of clicks of the mouse, you should be able to find what the name had originally been, who named it and when, and where it was published, as well as its current name (acccording to this website), if different from the name on our chart, and all the names it has been given over the years. The example given for the toothed representative in the Bolete Clade, for example, is Hydnomerulius. A check with IndexFungorum shows that Hydnomerulius pinastri (Fr.) Jarosch & Besl was published in 2001. The website lists the publication. It also lists its "current" name as Leucogyrophana pinastri (Fr.) Ginns & Weresub, which was published in 1976. We are using Hydnomerulius on this chart because in David Hibbett's MOR website we find both names (Hydnomerulius and Leucogyrophana) being used for this species, and we've chosen here to use Hydnomerulius). Tracing the name back, we find that there have been 9 names in all used for this one species. Burt in 1917 named it Merulius pinastri (Fr.) Burt, but it was originally described by Fries as Hydnum pinastri Fr. In 1814. It Is a resupinate fungus with tooth-like projections, not looking like anything we would call a Hydnum today.
This chart is in continuous development. As DNA sequences add new taxa or remove taxa previously but mistakenly understood to belong to a given clade, the changes will appear on this chart.
The Clade/Morphology Chart
Click to open the Homobasidiomycete chart in a new window.
Homobasidiomycete Phylogenetics and Taxonomy
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Comments, corrections, and additions should go to Gary Lincoff.